Ann. For. Sci. 63 (2006) 645–652
c INRA, EDP Sciences, 2006
DOI: 10.1051/forest:2006041
645
Review
Impact of summer drought on forest biodiversity: what do we know?
Frédéric Aa *, Volkmar Wb
b
a
Cemagref, Domaine des Barres, 45290 Nogent sur Vernisson, France
Justus-Liebig-University of Giessen, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany
(Received 14 October 2005; accepted 16 March 2006 )
Abstract – To date, very few studies have assessed the impact of summer droughts on forest biodiversity and ecosystem functioning. Decreased
ecosystem productivity and increased mortality are general consequences of drought on biodiversity. Competitive species, species adapted to cold and
wet conditions as well as species with low reproduction rates and/or limited mobility seem the more affected. However, species-specific effects are
regulated by mechanisms allowing for resistance to drought. The short-term consequences of drought on biodiversity depend on species abilities to
resist, and to recover after, drought, and on competitive interactions between species. Although the abundance of many species generally decreases
during drought, some taxa may increase in number during drought or shortly after. The effects of recurrent droughts must be evaluated in the wider
context of global climate and habitat change. Considering the predicted increase in drought frequency and intensity, interdisciplinary research initiatives
on this issue are needed urgently.
drought impact / biodiversity / forests / ecosystem functioning / global change
Résumé – Impact de la sécheresse estivale sur la biodiversité forestière : que savons-nous ? On connaît mal les conséquences des sécheresses sur la
biodiversité et le fonctionnement des écosystèmes forestiers. La productivité des écosystèmes semble diminuer et s’accompagne d’une mortalité accrue.
Les espèces compétitives, liées à des habitats frais ou humides, avec un faible taux de reproduction et/ou une mobilité réduite semblent les plus sensibles
à la sécheresse. La réponse spécifique dépend également des mécanismes de résistance à la sécheresse. Les conséquences à court terme dépendent de la
capacité des espèces à résister et à se rétablir de la sécheresse, et de leurs interactions. Un nombre conséquent de taxons peuvent être plus abondants en
période de sécheresse ou peu de temps après. Les effets de sécheresses récurrentes sont à replacer dans le cadre du changement climatique global et des
modifications d’habitats. Sachant que la fréquence et l’intensité des sécheresses devraient croître dans l’avenir, il est urgent de lancer des recherches
interdisciplinaires sur le sujet.
sécheresse / biodiversité / forêts / fonctionnement de l’écosystème / changement global
1. INTRODUCTION
The importance of natural hazards in shaping biodiversity has received renewed scientific attention. Experts agree
that natural disturbances will increase in frequency and intensity over the next few decades in response to global warming [52]. Both empirical and theoretical work has shown that
the frequency and intensity of disturbances influence biodiversity [80, 110].
The dramatic effects of the extreme summer drought in
2003 on trees in Western Europe (i.e. mortality, dieback, premature leaf fall) [23] highlight the need to assess the impact
of drought on forest biodiversity. All levels of forest biota
may be affected, including aboveground (e.g. trees, understory
layer) and belowground (e.g. soil microbiota, edaphic invertebrates) species that are intimately related. Therefore, drought
may have serious consequences for forest ecosystem functioning.
While scientific interest concerning the impact of global
warming on terrestrial ecosystems has increased recently [85,
108], the effects of extreme climatic events on forest ecosystems are still poorly understood [42]. To date, only a few stud* Corresponding author: [email protected]
ies have focused on the effects of drought on forest biodiversity (e.g. forest trees [46, 104]). Even studies attempting to
quantify the loss of wood volume following natural disasters
have not considered the direct effects of droughts [89, 104].
Investigations on the biological impacts of drought events
have focused mainly on arid, semi-arid, and Mediterranean
biomes and are biased towards open habitats such as grasslands. Extrapolating results from these habitats to temperate
forests is unlikely to be valid. A further limitation is that
most existing studies have concentrated on plants (especially
trees in temperate regions), pests and herbivorous insects. The
conclusions drawn from a few well-studied groups (plants, insects) should not be ‘blindly’ extrapolated to other components of biodiversity. In addition, most data on which our current knowledge is based are derived from experiments rather
than from observations. While experiments simplify the complex feedback systems found in natural conditions, observations generally lack replication and tend to be very short-term.
Thus, both approaches are necessary to compensate for their
respective shortcomings.
Herein, we summarize the literature on the impact of summer drought on terrestrial biodiversity, with emphasis on forest ecosystems. First, the factors predisposing an organism to
Article published by EDP Sciences and available at http://www.edpsciences.org/forest or http://dx.doi.org/10.1051/forest:2006041
646
F. Archaux, V. Wolters
Table I. Mechanisms of drought resistance.
Organism
Mechanisms
Animals
Thermo-regulation
Moving to more protected areas
Summer diapause
Stomatal closure
Production of antioxidant and compatible
compounds Changes in cell membrane composition
Rapid defoliation
Morphological adaptation (e.g. deep-rooting)
Seed bank
Plants
drought or, conversely, conferring drought-resistance are reviewed. Second, the short- (one or two years after the drought
event) and mid-term (a decade or so) consequences of drought
on biodiversity are assessed. Third, the long-term (decades or
more) consequences of drought combined with other global
changes on biodiversity are considered. There is evidence
that drought effects may be less severe during summer than
during other seasons of the year [39]. However, this review
examines the effects of summer drought events only. Intensity [35,91], duration [30] and frequency [79] of droughts also
influence biodiversity, with data suggesting that the duration of
a drought event may be more important than its intensity [30]
and that the impact of a single extreme drought may depend on
the overall temporal trend in drought intensity [54]. Extreme
temperatures, usually associated with summer drought, also
amplify environmental stress [5]. Unfortunately, these issues
cannot be covered here due to the limited number of adequate
studies (but see [11] for details on eco-physiology).
2. DROUGHT RESISTANCE AND PREDISPOSING
FACTORS
Table I summarizes resistance mechanisms of animals and
plants. Organisms can cope with drought/heat by escaping
these conditions (e.g. by moving in shaded areas) and/or by
alleviating the damaging effect of the physiological stress
(e.g. by producing compatible compounds to limit the osmotic stress). Details on physiological adaptation to drought
by plants can be found in [7, 11, 112], by insects in [4] and by
vertebrates in [69]. Analogies can be drawn between diapausing insects and seeds stored in a seed bank. In insects, summer
diapause aims primarily at escaping drought and may occur at
all developmental stages (from larval to adult) and may be facultative or not. Different environmental factors such as number
of daylight hours or temperature may lengthen or terminate the
diapause in a species-specific way [4, 51, 59].
Many factors can predispose organisms to drought in the
short- and mid-term (Tab. II). These factors are difficult to
summarize because of sparse and sometimes conflicting evidence. Moreover, some of the supposed ‘predisposing factors’
have never been scientifically proven.
At the individual level, the effects of drought may be influenced by genotype, age and location. Indeed, very young
or very old individuals are typically the primary victims of
drought events. Furthermore, individuals at the southern limits
of their geographical distribution may be particularly affected
by drought, as a species range is often determined by its physiological tolerance. Forest management that maximises leaf
area index and/or favours species in regions close to the maximal heat- or water stress-tolerance limits of the species may
threaten entire forest stands [45]. At the species level, the effects of drought are influenced by life history and ecological
traits, such as anatomical or morphological adaptations (e.g.
leaf size, depth of roots, Tab. II). At the ecosystem scale, the
main effects of drought may occur indirectly, with droughts
promoting the occurrence and/or increasing the intensity of
other natural or anthropogenic pressures. One of the most
striking examples is the dramatic increase of Mediterranean
forest fires during dry years. The higher likelihood of insect
attacks on water-stressed plants or trees is not a universal phenomenon (e.g. [16, 44]), but boring and sucking insects usually perform better on stressed plants (the contrary has been
reported for gall-making and chewing insects [24, 56]).
There seems to be a general consensus that species-poor
ecosystems are usually more sensitive to perturbations, such
as droughts, than species-rich ecosystems [50]. For instance,
a positive relationship was found between total biomass and
species richness of naturally co-occurring mosses and liverworts under experimental drought conditions but not under
constant conditions [73]. One explanation for the positive relationship between species richness and overall drought resistance may be that impoverished ecosystems may host fewer
species or groups that are capable of a differential functional
response [70]. For instance, a decrease in both total abundance and species richness of Collembola communities is associated with a strong reduction in decomposition rate [82].
However, ecosystem resistance and resilience are often unrelated to total species richness, the number of plant functional groups or the number of trophic levels (e.g. [109]). For
instance, high functional redundancy has been found among
forest soil microarthropods, so that the positive relationship
between species richness and ecosystem functions would appear only for very low values of species richness [62]. Several
studies have even emphasized the species-specific drought response of plants [14, 66], root mycorrhizae [55] and butterflies [92]. Idiosyncratic responses suggest that simple physiological models may not be sufficient to predict the effect
of drought on whole communities [21, 38]. Furthermore, response patterns at the community level are also regulated
by complex interactions between the different components of
trophic chains. For example, a greater abundance of insect
parasitoids and arthropod predators of European corn borer
larvae (Ostrinia nubilialis Hubner) in drought-stressed corn
fields compensated for the corn’s greater susceptibility to the
larvae [38].
3. SHORT- AND MID-TERM EFFECTS
OF DROUGHT
Observed and potential short- and mid-term impacts of a
drought event are listed in Table III. Short-term responses
may differ from mid- and long-term responses because (1)
Summer drought and forest biodiversity
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Table II. Observed and potential (in italics) factors predisposing taxa to drought impact. A distinction is made between factors that may vary
between individuals of the same species, between phylogenetically-related species (but not between individuals of the same species) or between
ecosystems (but not between species within the same ecosystem).
Level
Predisposing factor
Taxa and references
Individual
Location near species’ range boundary
Location in a shaded place
Age (young and old individuals)
Not entering diapause (when facultative)
Drought intolerant genotype
Tree [22], butterflies [99]
Plants [76, 107]
Trees [28, 61, 79]
Grassland flies [74]
Never demonstrated
Species
Large leaf-area
Competitive
Preference for cool or wet habitats
Absence of ground reserves
Trees [5, 18]
Temperate grassland herbs [25,72] but maybe not temperate forest understory
plants [71]
Forest plants [14, 106], temperate Carabids and butterflies but not moths [71]
Temperate herbaceous plants [15]
Temperate grassland herbs [14, 25, 72]
Temperate and Mediterranean grassland herbs [15, 66, 72]
Temperate butterflies but not moths [71]
Temperate forest understory plants [33] but see [12, 26]1
Never demonstrated
Shallow roots
Low reproduction rate
Low mobility
Specific competition
Not diapausing
Ecosystem
Disturbed ecosystems
Susceptibility to fire
Susceptibility to chemicals
Susceptibility to pest attack and disease
Susceptibility to invasion
1
Temperate grassland herbs [14], temperate mosses [73], temperate forest
Collembolans [82]
Mediterranean shrubs [65], Mediterranean forest Carabids [31], Mediterranean birds [47]
Temperate forest and boreal grassland Collembolans [48, 58] but see [61]
Various plants and trees [17, 90] but see [16, 44]
Never demonstrated
This may depend on the soil properties [18], temperature [21] and level of water supply and on the aspect of plant performance examined [87].
the impact of a drought event may appear primarily during
a prolonged recovery phase rather than during the event itself [25, 42], and (2) resistance and resilience to drought may
be negatively linked, as was found for herbaceous plant communities [67]. In the latter study, five herbaceous communities representing a wide range of functional types were experimentally subjected to drought in Great Britain. Fast-growing
(resilient) species tended to be more sensitive to damage by
drought than slow-growing species [67].
Lower productivity (as measured as changes in biomass or
cover over time) and higher mortality are the most widespread
effects of drought on plants. In two prairie grasslands, a major drought caused the annual production, which had been
nearly constant previously, to oscillate every two years for
at least nine years after the event, showing that drought
impact on ecosystem productivity may last far beyond the
event itself [43]. More fertile, early-successional ecosystems
may be more vulnerable to drought, as found for British
grasslands [41].
As for plants, desiccation during drought periods may increase the mortality rate of some insects [111], while other
species may remain largely unaffected [71, 88]. Drought may
even favour some taxa [68,71]. In fact, high temperatures usually stimulate an insect’s growth, allowing multivoltine species
(i.e. species that produce several broods in a single season) to
produce more generations per year. Furthermore, with the ex-
ception of species whose diapause is under strict photoperiodic
control [51], high temperatures may induce or extend summer
diapause [4]. Diapausing individuals are known to enjoy better survival and fecundity than non-diapausing ones [74, 113].
Information on the effects of the 2003 drought on forest insect
populations can be found in [86].
To date, data on the short- and mid-term consequences
of drought on biodiversity are almost completely confined to
studies in grasslands. Forest biodiversity, and especially vegetation, may be particularly resistant to drought. According to
annual surveys on 124 × 100 m2 plots of the French RENECOFOR long-term monitoring programme, for instance, changes
in community composition were small after the extreme 2003
drought (J.-L. Dupouey, pers. com.). A response, if any, is
more likely to result from canopy opening after drought [79]
than from the drought itself, with shifts in plant community
composition becoming apparent only several years after the
drought, until the canopy closes again. Current knowledge on
the impact of thinning cuts on herbaceous vegetation suggests
that small changes in canopy cover will probably increase the
number, the abundance and the flowering rate of forest plant
species [6, 100].
Another potential positive impact of drought on forest biodiversity relates to the increased amount of standing (snags)
and lying deadwood (branches, logs) [105]. Managed forests
are characterized by low deadwood volumes per ha compared
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F. Archaux, V. Wolters
Table III. Short- and mid-term, observed and potential (in italics), consequences of drought on biodiversity. A distinction is made between
factors operating primarily at the individual, species and ecosystem levels (see legend of Tab. II).
Level
Short-term consequences
Taxa and references
Individual
Reduced growth
Reduced fecundity
Increased mortality
Forest plants [39]
Plants [34], soil microarthropods [62], butterflies [84]
Trees [78] but see [71] for grassland herbs and insects
Species
Increase of deadwood-dwelling species
Shift in species range
Increase of drought-tolerant species
Saproxylic insect and fungi [24]
Never demonstrated
Never demonstrated
Ecosystem
Reduced productivity
Slower ecosystem functioning
Decrease in local species richness
Shift in species interactions
Shift in species composition
Boreal forest understory plants [13], temperate forest Collembolans [82],
boreal forest birds [8]
Temperate grassland herbs with accumulation of litter [25]
Boreal forest understory plants [75], temperate forest Collembolans [82]
Mountain grassland herbs [19]
Temperate grassland soil microarthropods [63]
Level
Mid-term consequences
Organisms and references
Individual
Lasting growth reduction
Delayed mortality
Susceptibility to pathogens and disease
Reduced offspring performance
Trees [76, 79, 97]
Trees [11, 78]
Trees [110]
Grassland moths (males that do not diapause [113])
Species
Increase of drought-tolerant species
Microevolutionary changes
Increase of deadwood-dwelling species
Shift in species range
Temperate forest understory plants [106]
Tropical island birds [10]
Never demonstrated
Never demonstrated
Ecosystem
Oscillations in productivity
Shift in species composition
Shift in species interactions
Reduced species richness
Temperate grassland herbs [43, 103]
Mountain grassland herbs [95]
Never demonstrated
Never demonstrated
to old-growth or primary forests [105]. Therefore, even a
small increase in deadwood in managed forests may have
considerable ecological consequences [37]. In Scandinavia,
about 25% of all forest species depend on deadwood (including fungi, insects, mosses, vertebrates and nematodes) [93].
Due to the lack of a global, standardised assessment of
drought susceptibility for even the most common animal
and plant taxa, the increase in drought-tolerant species after drought events has never been proven scientifically. For
instance, there is no Ellenberg-like [27] index for drought
resistance in vascular plants. Only surrogates for species
drought-tolerance such as preference for cool or wet habitats or morphological traits (e.g. ground reserves, root depth
for plants) have been used to assess the impact of droughts
(e.g. [14, 71]).
The assessment of species susceptibility to drought will be
an important step for understanding the impact of drought
on forest biodiversity but it probably will not be sufficient.
The response of communities to drought likely is more than
just the sum of the individual responses of species because
drought effects often are mediated through biological interactions. For example, drought may reduce the cover of
perennial plants (see above; [71]) or prevent colonisation of
poor soils by dominant plants [83]. This provides refuges
for tap-rooted plants [14] and allows rapid colonisation by
annuals or biannuals [15] from dormant or newly-dispersed
seeds [57]. In one alpine meadow site, dominant grasses decreased in cover following an extreme, 4-year drought period; they had not recovered their initial cover nine years
later because other species with a higher regenerative capacity had colonised [95]. In some cases, the identity of the
dominant species in the herb layer may be determined by
drought-resistance and competitive ability, with the outcome
depending on the relative importance of the two phenomena. For example, Bromus erectus Huds. is usually excluded
from calcareous grasslands in France by competition with
Brachypodium pinnatum (L.) Beauv., but dominates in areas
with high water-stress due to the greater drought sensitivity
Summer drought and forest biodiversity
of the latter species [19]. Relaxed inter-specific competition
probably explains why the richness of bryophytes in Southern Norwegian old-growth coniferous forests [75] and of vascular plants in British grasslands [71] increased shortly after
drought. Thus, an initial decrease in richness immediately after drought may be followed by an increase in richness, both at
very local (α diversity) and larger spatial scales (γ diversity),
either in a few years’ time and/or over a much longer time
period.
4. LONG-TERM EFFECTS OF DROUGHT
AND GLOBAL CHANGE
Drought frequency is thought to be the main driver of vegetation dynamics in Mediterranean [102], boreal [94, 101] and
temperate forests [64]. For example, the decline of oak in Europe has been linked to the detrimental effects of recurrent
droughts [60, 98]. Similarly, summer drought is thought to be
one of the factors that helped hazel to out-compete oak in the
southern Alps 11 000–10 500 cal yr BP [32]. Species can be
expected to shift their distribution in response to the new selection pressures, adapt or become extinct. Current changes
in geographic ranges of many species have been linked to
global warming in general, but extreme weather events, such
as droughts, provide an alternative explanation [77].
Extreme events such as droughts may generate intense
episodes of natural selection [3, 42]. Selection for droughttolerant genotypes may thus cause micro-evolutionary
changes. However, evidence for natural selection acting upon
a heritable variation in traits increasing drought tolerance is
lacking (but see [10]), although populations exposed to different drought frequencies often have corresponding levels of
drought–tolerance that are genetically fixed. Examples can be
found in [1, 53, 81] for plants and in [92] for insects. The flora
and fauna that still exists in the Northern Hemisphere survived
extreme climatic episodes during the Pleistocene. Therefore,
contemporary climatic changes can be expected to cause relatively few extinctions. However, most extant taxa in the Northern Hemisphere have been selected to resist winter cold rather
than summer drought or extreme heat (see [96] for plants
and [9] for birds). Furthermore, the genus-level conservatism
in climatic requirements observed in Northern Hemisphere
tree species [96] and the selection acting simultaneously on
antagonistic traits (e.g. dispersal/survival and fecundity, stressresistance and resilience) [29] may well prevent species from
adapting to rapidly changing environmental conditions. Additionally, the combinations of conditions that exist today may
change in the future, with past and present climatic conditions
failing to provide a suitable analogue. These changes may lead
to combinations of species that have never co-occurred before [2]. Finally, long-term impacts of droughts will depend
not only on drought frequency and intensity, but will be intimately linked to the effects of other atmospheric, climatic and
habitat changes also. Most of these changes interact in complex ways [36, 39]. For instance, high rates of atmospheric nitrogen deposition may reduce inter-specific plant competition
whilst a slow climatic warming may have little effect [40].
649
Overall, therefore, we lack sufficient data for making reliable predictions on the adaptive potential of species to the
simultaneous action of several drivers of global change [49].
5. CONCLUSION AND RESEARCH NEEDS
Drought is certainly a widely underestimated ecological
stress and selection force [42]. Our review has revealed a number of issues that should have priority in future research:
1. Variations of factors such as drought intensity, duration
and return frequency, species-specific phenotypic plasticity, adaptive potential and phylogenetic and physiological
constraints must be experimentally identified in relation to
drought events. This should lead to a concise classification
of species according to their sensitivity to drought or to
environmental features linked to drought. Particular focus
must be on vulnerable species and ecosystems, because
these will probably be the first to be seriously affected by
drought.
2. The impact of drought on ecosystem processes must be
studied to better understand how drought alters ecological
functions and how these effects are influenced by species
composition. Points 1 and 2 should help to define an indicator system for predicting drought sensitivity at the stand
and forest levels.
3. Research should focus on the simultaneous effects of
drought and other factors, such as forest management,
pollution and global warming. This is essential for identifying the most relevant factors that mediate the impact of drought events on forest biodiversity. The impact
of strategies that are being proposed to mitigate the effects of drought on trees on forest biodiversity should be
rapidly evaluated, especially the impact of the plantation
of drought-tolerant tree species and of the reduction of the
rotation length [20].
4. Long-term monitoring programs should be continued or
developed, since these are the only way for evaluating
the impact of rare events on ecosystems. However, these
programs should be coupled with integrative experimental
and modelling approaches to enhance our understanding
of complex drought effects.
5. The effects of drought events on forest biodiversity should
be considered in both planning (e.g. tree species selection)
and management (e.g. retention of deadwood).
Acknowledgements: We would like to thank Christophe Bouget,
Mike D. Morecroft and G. Landmann and one referee for their constructive comments on an earlier version of this paper.
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